The enigmatic cytoplasmic regions of KCNH channels

Journal of Molecular Biology

Volumn 427, Issue 1, 2015, Pages 67-76

  Morais Cabral, João H ^a   Robertson, Gail A ^b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

CNBh domains; ether go go; KCNH; PAS; potassium channels

Indexed keywords

POTASSIUM CHANNEL KCNH; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; KCNH1 PROTEIN, HUMAN; KCNH1 PROTEIN, MOUSE; POTASSIUM CHANNEL HERG;

CELL FUNCTION; CNBH DOMAIN; CYTOARCHITECTURE; CYTOPLASM; CYTOSOL; HUMAN; NONHUMAN; PAS DOMAIN; PROTEIN STRUCTURE; REVIEW; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM;

ANIMALS; CYTOPLASM; ETHER-A-GO-GO POTASSIUM CHANNELS; HUMANS; MODELS, MOLECULAR;

EID: 84919618793     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.08.008     Document Type: Review

References (81)

1. J.W. Warmke, and B. Ganetzky A family of potassium channel genes related to eag in Drosophila and mammals Proc Natl Acad Sci U S A 91 1994 3438 3442
2. J. Warmke, R. Drysdale, and B. Ganetzky A distinct potassium channel polypeptide encoded by the Drosophila eag locus Science 252 1991 1560 1562
3. M.C. Sanguinetti, and M. Tristani-Firouzi hERG potassium channels and cardiac arrhythmia Nature 440 2006 463 469
4. O. Crociani, L. Guasti, M. Balzi, A. Becchetti, E. Wanke, and M. Olivotto Cell cycle-dependent expression of HERG1 and HERG1B isoforms in tumor cells J Biol Chem 278 2003 2947 2955
5. L.A. Pardo, and W. Stuhmer The roles of K(+) channels in cancer Nat Rev Cancer 14 2014 39 48
6. S.J. Huffaker, J. Chen, K.K. Nicodemus, F. Sambataro, F. Yang, and V. Mattay A primate-specific, brain isoform of KCNH2 affects cortical physiology, cognition, neuronal repolarization and risk of schizophrenia Nat Med 15 2009 509 518
7. X. Zhang, F. Bertaso, J.W. Yoo, K. Baumgartel, S.M. Clancy, and V. Lee Deletion of the potassium channel Kv12.2 causes hippocampal hyperexcitability and epilepsy Nat Neurosci 13 2010 1056 1058
8. J. Ludwig, H. Terlau, F. Wunder, A. Bruggemann, L.A. Pardo, and A. Marquardt Functional expression of a rat homologue of the voltage gated either a go-go potassium channel reveals differences in selectivity and activation kinetics between the Drosophila channel and its mammalian counterpart EMBO J 13 1994 4451 4458
9. G.A. Robertson, J.M. Warmke, and B. Ganetzky Potassium currents expressed from Drosophila and mouse eag cDNAs in Xenopus oocytes Neuropharmacology 35 1996 841 850
10. S.L. Wynia-Smith, A.L. Gillian-Daniel, K.A. Satyshur, and G.A. Robertson hERG gating microdomains defined by S6 mutagenesis and molecular modeling J Gen Physiol 132 2008 507 520
11. S. Thouta, S. Sokolov, Y. Abe, S.J. Clark, Y.M. Cheng, and T.W. Claydon Proline scan of the HERG channel S6 helix reveals the location of the intracellular pore gate Biophys J 106 2014 1057 1069
12. H.R. Guy, S.R. Durell, J. Warmke, R. Drysdale, and B. Ganetzky Similarities in amino acid sequences of Drosophila eag and cyclic nucleotide-gated channels Science 254 1991 730
13. J.H. Morais Cabral, A. Lee, S.L. Cohen, B.T. Chait, M. Li, and R. Mackinnon Crystal structure and functional analysis of the HERG potassium channel N terminus: a eukaryotic PAS domain Cell 95 1998 649 655
14. B.E. McIntosh, J.B. Hogenesch, and C.A. Bradfield Mammalian Per-Arnt-Sim proteins in environmental adaptation Annu Rev Physiol 72 2010 625 645
15. A. Moglich, R.A. Ayers, and K. Moffat Structure and signaling mechanism of Per-ARNT-Sim domains Structure 17 2009 1282 1294
16. J.T. Henry, and S. Crosson Ligand-binding PAS domains in a genomic, cellular, and structural context Annu Rev Microbiol 65 2011 261 286
17. M.J. Marques-Carvalho, N. Sahoo, F.W. Muskett, R.S. Vieira-Pires, G. Gabant, and M. Cadene Structural, biochemical, and functional characterization of the cyclic nucleotide binding homology domain from the mouse EAG1 potassium channel J Mol Biol 423 2012 34 46
18. T.I. Brelidze, A.E. Carlson, B. Sankaran, and W.N. Zagotta Structure of the carboxy-terminal region of a KCNH channel Nature 481 2012 530 533
19. H. Rehmann, A. Wittinghofer, and J.L. Bos Capturing cyclic nucleotides in action: snapshots from crystallographic studies Nat Rev Mol Cell Biol 8 2007 63 73
20. B. Nan, X. Liu, Y. Zhou, J. Liu, L. Zhang, and J. Wen From signal perception to signal transduction: ligand-induced dimeric switch of DctB sensory domain in solution Mol Microbiol 75 2010 1484 1494
21. M.C. Sanguinetti, C. Jiang, M.E. Curran, and M.T. Keating A mechanistic link between an inherited and an acquired cardiac arrhythmia: HERG encodes the IKr potassium channel Cell 81 1995 299 307
22. M.C. Trudeau, J.W. Warmke, B. Ganetzky, and G.A. Robertson HERG, a human inward rectifier in the voltage-gated potassium channel family Science 269 1995 92 95
23. + current is composed of two currents in guinea pig atrial cells Am J Physiol 260 1991 H393 H399
24. Z. Zhou, Q. Gong, B. Ye, Z. Fan, J.C. Makielski, and G.A. Robertson Properties of HERG channels stably expressed in HEK 293 cells studied at physiological temperature Biophys J 74 1998 230 241
25. R. Schonherr, and S.H. Heinemann Molecular determinants for activation and inactivation of HERG, a human inward rectifier potassium channel J Physiol 493 1996 635 642
26. P.S. Spector, M.E. Curran, A. Zou, M.T. Keating, and M.C. Sanguinetti Fast inactivation causes rectification of the IKr channel J Gen Physiol 107 1996 611 619
27. J. Wang, C.D. Myers, and G.A. Robertson Dynamic control of deactivation gating by a soluble amino-terminal domain in HERG K(+) channels J Gen Physiol 115 2000 749 758
28. J. Chen, A. Zou, I. Splawski, M.T. Keating, and M.C. Sanguinetti Long QT syndrome-associated mutations in the Per-Arnt-Sim (PAS) domain of HERG potassium channels accelerate channel deactivation J Biol Chem 274 1999 10113 10118
29. C.A. Harley, C.S. Jesus, R. Carvalho, R.M. Brito, and J.H. Morais-Cabral Changes in channel trafficking and protein stability caused by LQT2 mutations in the PAS domain of the HERG channel PLoS One 7 2012 e32654
30. E.C. Gianulis, and M.C. Trudeau Rescue of aberrant gating by a genetically encoded PAS (Per-Arnt-Sim) domain in several long QT syndrome mutant human ether-a-go-go-related gene potassium channels J Biol Chem 286 2011 22160 22169
31. R. Adaixo, and J.H. Morais-Cabral Crystallization and preliminary crystallographic characterization of the PAS domains of EAG and ELK potassium channels Acta Crystallogr Sect F Struct Biol Cryst Commun 66 2010 1056 1059
32. Q. Li, S. Gayen, A.S. Chen, Q. Huang, M. Raida, and C. Kang NMR solution structure of the N-terminal domain of hERG and its interaction with the S4-S5 linker Biochem Biophys Res Commun 403 2010 126 132
33. C.A. Ng, M.J. Hunter, M.D. Perry, M. Mobli, Y. Ke, and P.W. Kuchel The N-terminal tail of hERG contains an amphipathic alpha-helix that regulates channel deactivation PLoS One 6 2011 e16191
34. + channel deactivation gating from the solution structure of the EAG domain J Biol Chem 286 2011 6184 6191
35. R. Adaixo, C.A. Harley, A.F. Castro-Rodrigues, and J.H. Morais-Cabral Structural properties of PAS domains from the KCNH potassium channels PLoS One 8 2013 e59265
36. J. Wang, M.C. Trudeau, A.M. Zappia, and G.A. Robertson Regulation of deactivation by an amino terminal domain in human ether-a-go-go-related gene potassium channels J Gen Physiol 112 1998 637 647
37. P. de la Pena, C. Alonso-Ron, A. Machin, J. Fernandez-Trillo, L. Carretero, and P. Dominguez Demonstration of physical proximity between the N terminus and the S4-S5 linker of the human ether-a-go-go-related gene (hERG) potassium channel J Biol Chem 286 2011 19065 19075
38. H. Terlau, S.H. Heinemann, W. Stuhmer, O. Pongs, and J. Ludwig Amino terminal-dependent gating of the potassium channel rat eag is compensated by a mutation in the S4 segment J Physiol 502 1997 537 543
39. T.I. Brelidze, A.E. Carlson, and W.N. Zagotta Absence of direct cyclic nucleotide modulation of mEAG1 and hERG1 channels revealed with fluorescence and electrophysiological methods J Biol Chem 284 2009 27989 27997
40. T.I. Brelidze, E.C. Gianulis, F. DiMaio, M.C. Trudeau, and W.N. Zagotta Structure of the C-terminal region of an ERG channel and functional implications Proc Natl Acad Sci U S A 110 2013 11648 11653
41. C. Levy, K. Pike, D.J. Heyes, M.G. Joyce, K. Gabor, and H. Smidt Molecular basis of halorespiration control by CprK, a CRP-FNR type transcriptional regulator Mol Microbiol 70 2008 151 167
42. W.N. Lanzilotta, D.J. Schuller, M.V. Thorsteinsson, R.L. Kerby, G.P. Roberts, and T.L. Poulos Structure of the CO sensing transcription activator CooA Nat Struct Biol 7 2000 876 880
43. A.E. Carlson, T.I. Brelidze, and W.N. Zagotta Flavonoid regulation of EAG1 channels J Gen Physiol 141 2013 347 358
44. K.B. Craven, and W.N. Zagotta CNG and HCN channels: two peas, one pod Annu Rev Physiol 68 2006 375 401
45. W.N. Zagotta, N.B. Olivier, K.D. Black, E.C. Young, R. Olson, and E. Gouaux Structural basis for modulation and agonist specificity of HCN pacemaker channels Nature 425 2003 200 205
46. K.B. Craven, and W.N. Zagotta Salt bridges and gating in the COOH-terminal region of HCN2 and CNGA1 channels J Gen Physiol 124 2004 663 677
47. J.P. Johnson, and W.N. Zagotta The carboxyl-terminal region of cyclic nucleotide-modulated channels is a gating ring, not a permeation path Proc Natl Acad Sci U S A 102 2005 2742 2747
48. L. Hua, and S.E. Gordon Functional interactions between A′ helices in the C-linker of open CNG channels J Gen Physiol 125 2005 335 344
49. Y. Haitin, A.E. Carlson, and W.N. Zagotta The structural mechanism of KCNH-channel regulation by the eag domain Nature 501 2013 444 448
50. A.S. Gustina, and M.C. Trudeau HERG potassium channel regulation by the N-terminal eag domain Cell Signal 24 2012 1592 1598
51. L. Stevens, M. Ju, and D. Wray Roles of surface residues of intracellular domains of heag potassium channels Eur Biophys J 38 2009 523 532
52. A.S. Gustina, and M.C. Trudeau A recombinant N-terminal domain fully restores deactivation gating in N-truncated and long QT syndrome mutant hERG potassium channels Proc Natl Acad Sci U S A 106 2009 13082 13087
53. A.S. Gustina, and M.C. Trudeau The eag domain regulates hERG channel inactivation gating via a direct interaction J Gen Physiol 141 2013 229 241
54. A.S. Gustina, and M.C. Trudeau hERG potassium channel gating is mediated by N- and C-terminal region interactions J Gen Physiol 137 2011 315 325
55. E.C. Gianulis, Q. Liu, and M.C. Trudeau Direct interaction of eag domains and cyclic nucleotide-binding homology domains regulate deactivation gating in hERG channels J Gen Physiol 142 2013 351 366
56. + current Circ Res 81 1997 870 878
57. + channel in mouse and human hearts Circ Res 81 1997 719 726
58. P. Phartiyal, E.M. Jones, and G.A. Robertson Heteromeric assembly of human ether-a-go-go-related gene (hERG) 1a/1b channels occurs cotranslationally via N-terminal interactions J Biol Chem 282 2007 9874 9882
59. H. Sale, J. Wang, T.J. O'Hara, D.J. Tester, P. Phartiyal, and J.Q. He Physiological properties of hERG 1a/1b heteromeric currents and a hERG 1b-specific mutation associated with Long-QT syndrome Circ Res 103 2008 e81 e95
60. E.M. Jones, E.C. Roti Roti, J. Wang, S.A. Delfosse, and G.A. Robertson Cardiac IKr channels minimally comprise hERG 1a and 1b subunits J Biol Chem 279 2004 44690 44694
61. L. Crotti, D.J. Tester, W.M. White, D.C. Bartos, R. Insolia, and A. Besana Long QT syndrome-associated mutations in intrauterine fetal death JAMA 309 2013 1473 1482
62. A.P. Larsen, S.P. Olesen, M. Grunnet, and T. Jespersen Characterization of hERG1a and hERG1b potassium channels-a possible role for hERG1b in the I (Kr) current Pflugers Arch 456 2008 1137 1148
63. X. Wang, R. Xu, G. Abernathey, J. Taylor, M.B. Alzghoul, and K. Hannon Kv11.1 channel subunit composition includes MinK and varies developmentally in mouse cardiac muscle Dev Dyn 237 2008 2430 2437
64. + channel polypeptide is encoded by the seizure locus J Neurosci 17 1997 875 881
65. T. Fergestad, H. Sale, B. Bostwick, A. Schaffer, L. Ho, and G.A. Robertson A Drosophila behavioral mutant, down and out (dao), is defective in an essential regulator of Erg potassium channels Proc Natl Acad Sci U S A 107 2010 5617 5621
66. A.S. Martinson, D.B. van Rossum, F.H. Diatta, M.J. Layden, S.A. Rhodes, and M.Q. Martindale Functional evolution of Erg potassium channel gating reveals an ancient origin for IKr Proc Natl Acad Sci U S A 111 2014 5712 5717
67. C.G. Viloria, F. Barros, T. Giraldez, D. Gomez-Varela, and P. de la Pena Differential effects of amino-terminal distal and proximal domains in the regulation of human erg K(+) channel gating Biophys J 79 2000 231 246
68. J. Ludwig, D. Owen, and O. Pongs Carboxy-terminal domain mediates assembly of the voltage-gated rat ether-a-go-go potassium channel EMBO J 16 1997 6337 6345
69. M. Jenke, A. Sanchez, F. Monje, W. Stuhmer, R.M. Weseloh, and L.A. Pardo C-terminal domains implicated in the functional surface expression of potassium channels EMBO J 22 2003 395 403
70. I.H. Chen, J.H. Hu, G.M. Jow, C.C. Chuang, T.T. Lee, and D.C. Liu Distal end of carboxyl terminus is not essential for the assembly of rat Eag1 potassium channels J Biol Chem 286 2011 27183 27196
71. R. Schonherr, K. Lober, and S.H. Heinemann Inhibition of human ether a go-go potassium channels by Ca(2 +)/calmodulin EMBO J 19 2000 3263 3271
72. 2 +/calmodulin binding to the cytosolic N- and C-termini FEBS J 273 2006 1074 1086
73. J.T. Goncalves, and W. Stuhmer Calmodulin interaction with hEAG1 visualized by FRET microscopy PLoS One 5 2010 e10873
74. Z. Wang, G.F. Wilson, and L.C. Griffith Calcium/calmodulin-dependent protein kinase II phosphorylates and regulates the Drosophila eag potassium channel J Biol Chem 277 2002 24022 24029
75. X.X. Sun, J.J. Hodge, Y. Zhou, M. Nguyen, and L.C. Griffith The eag potassium channel binds and locally activates calcium/calmodulin-dependent protein kinase II J Biol Chem 279 2004 10206 10214
76. M. Sanhueza, and J. Lisman The CaMKII/NMDAR complex as a molecular memory Mol Brain 6 2013 10
77. E.C. Roti, C.D. Myers, R.A. Ayers, D.E. Boatman, S.A. Delfosse, and E.K. Chan Interaction with GM130 during HERG ion channel trafficking. Disruption by type 2 congenital long QT syndrome mutations. Human Ether-a-go-go-Related Gene J Biol Chem 277 2002 47779 47785
78. + channel in a lipid membrane-like environment Nature 450 2007 376 382
79. M.H. Akabas, D.A. Stauffer, M. Xu, and A. Karlin Acetylcholine receptor channel structure probed in cysteine-substitution mutants Science 258 1992 307 310
80. R.B. Bass, S.L. Butler, S.A. Chervitz, S.L. Gloor, and J.J. Falke Use of site-directed cysteine and disulfide chemistry to probe protein structure and dynamics: applications to soluble and transmembrane receptors of bacterial chemotaxis Methods Enzymol 423 2007 25 51
81. I.M. Herzberg, M.C. Trudeau, and G.A. Robertson Transfer of rapid inactivation and sensitivity to the class III antiarrhythmic drug E-4031 from HERG to M-eag channels J Physiol 511 1998 3 14